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Volume 16, Number 14, Issue of July 15, 1996 pp. 4344-4359
Copyright ©1996 Society for Neuroscience

[Ca²⁺]_i Elevations Detected by BK Channels during Ca²⁺ Influx and Muscarine-Mediated Release of Ca²⁺ from Intracellular Stores in Rat Chromaffin Cells

Received Nov. 7, 1995; revised April 18, 1996; accepted April 23, 1996.

Murali Prakriya, Christopher R. Solaro, and Christopher J. Lingle

Washington University School of Medicine, Department of Anesthesiology, St. Louis, Missouri 63110

Submembrane [Ca²⁺]_i changes were examined in rat chromaffin cells by monitoring the activity of an endogenous Ca²⁺-dependent protein: the large conductance Ca²⁺- and voltage-activated K⁺ channel (also known as the BK channel). The Ca²⁺ and voltage dependence of BK current inactivation and conductance were calibrated first by using defined [Ca²⁺]_i salines. This information was used to examine submembrane [Ca²⁺]_i elevations arising out of Ca²⁺ influx and muscarine-mediated release of Ca²⁺ from intracellular stores. During Ca²⁺ influx, some BK channels are exposed to [Ca²⁺]_i of at least 60 µM. However, the distribution of this [Ca²⁺]_i elevation is highly nonuniform so that the average [Ca²⁺]_i detected when all BK channels are activated is only ~10 µM. Intracellular dialysis with 1 mM or higher EGTA spares only the BK channels activated by the highest [Ca²⁺]_i during influx, whereas dialysis with 1 mM or higher BAPTA blocks activation of all BK channels. Submembrane [Ca²⁺]_i elevations fall rapidly after termination of short (5 msec) Ca²⁺ influx steps but persist above 1 µM for several hundred milliseconds after termination of long (200 msec) influx steps. In contrast to influx, the submembrane [Ca²⁺]_i elevations produced by release of intracellular Ca²⁺ by muscarinic actetylcholine receptor (mAChR) activation are much more uniform and reach peak levels of 3-5 µM. Our results suggest that during normal action potential activity only 10-20% of BK channels in each chromaffin cell see sufficient [Ca²⁺]_i to be activated.

Key words: BK channels; calcium; calcium channels; calcium stores; chromaffin cells; catecholamine secretion; K⁺ channel inactivation

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